Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1982 Sep;151(3):1261–1268. doi: 10.1128/jb.151.3.1261-1268.1982

Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate.

J Ryals, R Little, H Bremer
PMCID: PMC220404  PMID: 6179924

Abstract

The expression of stable RNA (rRNA and tRNA) genes and the concentration of guanosine tetraphosphate (ppGpp) were measured in an isogenic pair of relA+ and relA derivatives of Escherichia coli B/r. The cells were either growing exponentially at different rates or subject to amino acid starvation when they were measured. The specific stable RNA gene activity (rs/rt, the rate of rRNA and tRNA synthesis relative to the total instantaneous rate of RNA synthesis) was found to decrease from 1.0 at a ppGpp concentration of 0 (extrapolated value) to 0.24 at saturating concentrations of ppGpp (above 100 pmoles per optical density at 460 nm unit of cell mass). The same relationship between the rs/rt ratio and ppGpp concentration was obtained independent of the physiological state of the bacteria (i.e., independent of the growth rate or of amino acid starvation) and independent of the relA allele. It can be concluded that ppGpp is an effector for stable RNA gene control and that stable RNA genes are not controlled by factors other than the ppGpp-mediated system. The results were shown to be qualitatively and quantitatively consistent with data on in vitro rRNA gene control by ppGpp, and they were interpreted in the light of reported ideas derived from those in vitro experiments.

Full text

PDF
1261

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Biebricher C. K., Druminski M. Inhibition of RNA polymerase activity by the Escherichia coli protein biosynthesis elongation factor Ts. Proc Natl Acad Sci U S A. 1980 Feb;77(2):866–869. doi: 10.1073/pnas.77.2.866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bremer H., Yuan D. RNA chain growth-rate in Escherichia coli. J Mol Biol. 1968 Dec 14;38(2):163–180. doi: 10.1016/0022-2836(68)90404-x. [DOI] [PubMed] [Google Scholar]
  3. Brunschede H., Dove T. L., Bremer H. Establishment of exponential growth after a nutritional shift-up in Escherichia coli B/r: accumulation of deoxyribonucleic acid, ribonucleic acid, and protein. J Bacteriol. 1977 Feb;129(2):1020–1033. doi: 10.1128/jb.129.2.1020-1033.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cashel M., Gallant J. Two compounds implicated in the function of the RC gene of Escherichia coli. Nature. 1969 Mar 1;221(5183):838–841. doi: 10.1038/221838a0. [DOI] [PubMed] [Google Scholar]
  5. Churchward G., Bremer H., Young R. Transcription in bacteria at different DNA concentrations. J Bacteriol. 1982 May;150(2):572–581. doi: 10.1128/jb.150.2.572-581.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dalbow D. G., Bremer H. Metabolic regulation of beta-galactosidase synthesis in Escherichia coli. A test for constitutive ribosome synthesis. Biochem J. 1975 Jul;150(1):1–8. doi: 10.1042/bj1500001b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dennis P. P., Bremer H. Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol. 1974 Jul;119(1):270–281. doi: 10.1128/jb.119.1.270-281.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fiil N. P., von Meyenburg K., Friesen J. D. Accumulation and turnover of guanosine tetraphosphate in Escherichia coli. J Mol Biol. 1972 Nov 28;71(3):769–783. doi: 10.1016/s0022-2836(72)80037-8. [DOI] [PubMed] [Google Scholar]
  9. Gallant J. A. Stringent control in E. coli. Annu Rev Genet. 1979;13:393–415. doi: 10.1146/annurev.ge.13.120179.002141. [DOI] [PubMed] [Google Scholar]
  10. Gallant J., Palmer L., Pao C. C. Anomalous synthesis of ppGpp in growing cells. Cell. 1977 May;11(1):181–185. doi: 10.1016/0092-8674(77)90329-4. [DOI] [PubMed] [Google Scholar]
  11. Hansen M. T., Pato M. L., Molin S., Fill N. P., von Meyenburg K. Simple downshift and resulting lack of correlation between ppGpp pool size and ribonucleic acid accumulation. J Bacteriol. 1975 May;122(2):585–591. doi: 10.1128/jb.122.2.585-591.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Haseltine W. A., Block R., Gilbert W., Weber K. MSI and MSII made on ribosome in idling step of protein synthesis. Nature. 1972 Aug 18;238(5364):381–384. doi: 10.1038/238381a0. [DOI] [PubMed] [Google Scholar]
  13. Haseltine W. A., Block R. Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci U S A. 1973 May;70(5):1564–1568. doi: 10.1073/pnas.70.5.1564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hughes J., Mellows G. Inhibition of isoleucyl-transfer ribonucleic acid synthetase in Escherichia coli by pseudomonic acid. Biochem J. 1978 Oct 15;176(1):305–318. doi: 10.1042/bj1760305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lagosky P. A., Chang F. N. Correlation between RNA synthesis and basal level guanosine 5'-diphosphate 3'-diphosphate in relaxed mutants of Escherichia coli. J Biol Chem. 1981 Nov 25;256(22):11651–11656. [PubMed] [Google Scholar]
  16. Lazzarini R. A., Cashel M., Gallant J. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J Biol Chem. 1971 Jul 25;246(14):4381–4385. [PubMed] [Google Scholar]
  17. Nierlich D. P. Regulation of ribonucleic acid synthesis in growing bacterial cells. II. Control over the composition of the newly made RNA. J Mol Biol. 1972 Dec 30;72(3):765–777. doi: 10.1016/0022-2836(72)90190-8. [DOI] [PubMed] [Google Scholar]
  18. Pao C. C., Dyess B. T. Stringent control of RNA synthesis in the absence of guanosine 5'-diphosphate-3'-diphosphate. J Biol Chem. 1981 Mar 10;256(5):2252–2257. [PubMed] [Google Scholar]
  19. Pao C. C., Gallant J. A new nucleotide involved in the stringent response in Escherichia coli. Guanosine 5'-diphosphate-3'-monophosphate. J Biol Chem. 1979 Feb 10;254(3):688–692. [PubMed] [Google Scholar]
  20. Rose J. K., Yanofsky C. Metabolic regulation of the tryptophan operon of Escherichia coli: repressor-independent regulation of transcription initiation frequency. J Mol Biol. 1972 Aug 14;69(1):103–118. doi: 10.1016/0022-2836(72)90026-5. [DOI] [PubMed] [Google Scholar]
  21. Ryals J., Bremer H. relA-dependent RNA polymerase activity in Escherichia coli. J Bacteriol. 1982 Apr;150(1):168–179. doi: 10.1128/jb.150.1.168-179.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ryals J., Little R., Bremer H. Temperature dependence of RNA synthesis parameters in Escherichia coli. J Bacteriol. 1982 Aug;151(2):879–887. doi: 10.1128/jb.151.2.879-887.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shen V., Bremer H. Rate of ribosomal ribonucleic acid chain elongation in Escherichia coli B/r during chloramphenicol treatment. J Bacteriol. 1977 Jun;130(3):1109–1116. doi: 10.1128/jb.130.3.1109-1116.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shepherd N. S., Churchward G., Bremer H. Synthesis and activity of ribonucleic acid polymerase in Escherichia coli. J Bacteriol. 1980 Mar;141(3):1098–1108. doi: 10.1128/jb.141.3.1098-1108.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Somerville C. R., Ahmed A. Mutants of Escherichia coli defective in the degradation of guanosine 5'-triphosphate, 3'-diphosphate (pppGpp). Mol Gen Genet. 1979 Feb 1;169(3):315–323. doi: 10.1007/BF00382277. [DOI] [PubMed] [Google Scholar]
  26. Spadaro A., Spena A., Santonastaso V., Conini P. Stringency without ppGpp accumulation. Nature. 1981 May 21;291(5812):256–258. doi: 10.1038/291256a0. [DOI] [PubMed] [Google Scholar]
  27. Travers A. A. A tRNATyr promoter with an altered in vitro response to ppgpp. J Mol Biol. 1980 Jul 25;141(1):91–97. doi: 10.1016/s0022-2836(80)80030-1. [DOI] [PubMed] [Google Scholar]
  28. Travers A. A., Buckland R., Goman M., Le Grice S. S., Scaife J. G. A mutation affecting the sigma subunit of RNA polymerase changes transcriptional specificity. Nature. 1978 Jun 1;273(5661):354–358. doi: 10.1038/273354a0. [DOI] [PubMed] [Google Scholar]
  29. Travers A. A., Debenham P. G., Pongs O. Translation initiation factor 2 alters transcriptional selectivity of Escherichia coli ribonucleic acid polymerase. Biochemistry. 1980 Apr 15;19(8):1651–1656. doi: 10.1021/bi00549a020. [DOI] [PubMed] [Google Scholar]
  30. Travers A. Modulation of RNA polymerase specificity by ppGpp. Mol Gen Genet. 1976 Aug 19;147(2):225–232. doi: 10.1007/BF00267575. [DOI] [PubMed] [Google Scholar]
  31. Travers A. RNA polymerase specificity and the control of growth. Nature. 1976 Oct 21;263(5579):641–646. doi: 10.1038/263641a0. [DOI] [PubMed] [Google Scholar]
  32. Travers A. RNA polymerase--promoter interactions: some general principles. Cell. 1974 Oct;3(2):97–104. doi: 10.1016/0092-8674(74)90112-3. [DOI] [PubMed] [Google Scholar]
  33. van Ooyen A. J., Gruber M., Jorgensen P. The mechanism of action of ppGpp on rRNA synthesis in vitro. Cell. 1976 May;8(1):123–128. doi: 10.1016/0092-8674(76)90193-8. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES